Clinician perceptions on barriers and facilitators to 1‐year surveillance colonoscopy completion in survivors of colorectal cancer

Abstract Introduction Colorectal cancer (CRC) is the second leading cause of cancer deaths in the United States. Surveillance colonoscopy is recommended 1‐year after surgical resection for patients with stage I‐III CRC; however, only 18%–61% of CRC survivors complete this test. This study describes clinician‐identified barriers and facilitators to surveillance colonoscopy among CRC survivors. Methods We conducted semi‐structured interviews with clinicians until thematic saturation was achieved. Interviews were analyzed using the social cognitive theory. Results Thirteen clinicians were interviewed, and all identified health system‐level barriers to surveillance colonoscopy completion; the most common being fragmented care due to patients receiving care across many health systems. Clinicians also identified social determinants of health barriers (e.g., geographical distance between patients and health systems) to 1‐year surveillance colonoscopy completion. Conclusions Clinicians identified several potentially modifiable barriers to 1‐year surveillance colonoscopy completion which, if addressed, could improve post‐treatment care and outcomes among stage I‐III CRC survivors.

risk of local recurrence, so understanding the potentially modifiable barriers and facilitators to surveillance colonoscopy completion is critical to improving care outcomes.
Few studies have evaluated the barriers and facilitators to surveillance colonoscopy completion in CRC survivors. 8,9Our prior analysis found that older age, higher stage CRC, and living without a partner were associated with lower adherence to surveillance colonoscopy. 10ther factors such as distance from an endoscopy suite also impact adherence. 11Many demographic and clinical factors identified to date are non-modifiable, and administrative claims data may not completely capture intervenable factors.Qualitative studies could fill the knowledge gap and inform interventions to address this issue.This study aimed to describe clinician-identified barriers and facilitators to 1-year surveillance colonoscopy completion.

| METHODS
We conducted semi-structured interviews of clinicians caring for CRC patients.We adhered to the Consolidated Criteria for Reporting Qualitative Research (COREQ) reporting guideline and the US Federal Policy for the Protection of Human Subjects. 12The study was approved by the Fred Hutchinson Cancer Center/University of Washington Cancer Consortium's Institutional Review Board.All participants provided consent and received a $100.00 cash incentive.

| Study setting, sampling and recruitment
Clinicians were recruited via email from the Hutchinson Institute for Cancer Outcomes Research (HICOR) Value in Cancer Care (VCC) network, an academic communityintegrated consortium of 217 medical oncologists from 14 health systems in Washington state (Data S1).Clinicians included medical oncologists, colorectal surgeons, gastroenterologists, and advanced practice providers (APPs) who were VCC clinic employees and ≥18 years old.Participants were recruited from two clinics with higher surveillance colonoscopy completion rates and one clinic with lower surveillance colonoscopy completion rates based on the 2021 HICOR Annual Quality Report and prior research. 10,13

| Interview guide development
We conducted grounded interviews using open-ended questions to explore beliefs and knowledge about surveillance colonoscopies. 14The semi-structured interview guide was developed by the study team and informed by the Health Belief Model (HBM). 15The HBM was developed to inform behaviors related to uptake of health services and was selected because of its extensive use in understanding barriers to CRC screening (Data S2).

| Data collection
Semi-structured interviews and demographic surveys were completed via a video-conferencing platform by authors T.H and C.N.K. Interviews were recorded, deidentified, and transcribed verbatim.Following accepted standards of rigor in qualitative research, we collected data until thematic saturation was reached. 16

| Data analysis
Descriptive data were reported as proportions or medians and interquartile ranges (IQRs).Three authors (C.N.K., A.B.B., and R.B.I.) developed an initial set of codes inductively and deductively informed by the social cognitive theory (SCT).8][19] Codes and definitions were discussed and modified across the research team prior to finalization.The lead coder (C.N.K) applied the codebook across interviews to identify key themes using the Dedoose qualitative coding software version 9.0.107(SocioCultural Research Consultants).

| Clinician characteristics
Twenty-one clinicians received an invitation to participate, 17 provided consent, and 13 completed interviews.Ten were physicians, and three were APPs (Table 1).Nine clinicians (69.2%) identified as female and 10 (76.9%) spent more than 75% of their time in direct patient care.Eight clinicians (61.5%) had a clinical practice size of greater than 100 CRC patients.

| Barriers to surveillance colonoscopy completion
Clinicians identified barriers to surveillance colonoscopy completion across two main themes-(1) health system-level barriers and (2) patient-level barriers.Themes and quotations are summarized in Table 2.

Organizational factors
The most frequently reported organizational factors were fragmented care (10 participants [76.9%]), workplace pressures (6 participants [46.2%]), and long wait times (6 participants [46.2%]).Clinicians commented that managing CRC patients across multiple institutions with non-integrated EHRs led to fragmented care.Workplace pressures (e.g., busy clinic schedules, competing medical issues during visits) hindered reminding patients about surveillance colonoscopy completion.

Clinician cognitive factors
The most reported clinician-identified cognitive barriers were differing expectations about which specialist had ownership of scheduling or tracking surveillance procedures (5 participants [38.5%]) and clinicians' lack of knowledge about guidelines (5 participants [38.5%]).
Clinicians acknowledged that relying on other colleagues like oncologists or primary care doctors to remind patients about their surveillance likely contributed to missed follow-up.Limited exposure to CRC patients among some clinicians also led to a lack of knowledge of surveillance requirements.

Social determinants of health
The most common patient-level SDOH barriers were geography (i.e., distance from home to the healthcare facility; 6 participants [46.2%]), health insurance (5 participants [38.5%]), other life obligations (5 participants [38.5%]), and lack of procedural transportation or a chaperone (4 participants [30.8%]).Clinicians commented that patients that lived farther from the health system faced challenges traveling for surveillance colonoscopies, especially while completing a bowel preparation.Similarly, transportation barriers and lack of a caregiver contributed to delays or missed appointments.

| Patient cognitive factors
The patient-centered cognitive factors identified as barriers included patients forgetting that they needed a surveillance colonoscopy (3 participants [23.1%]), patients thinking that their CRC management was complete after surgical resection (2 participants [15.4%]), and patients missing or delaying surveillance colonoscopies due to negative past experiences with endoscopy (2 participants [15.4%]).

Facilitators to surveillance colonoscopy completion
Facilitators to surveillance colonoscopy completion fell into two main themes-(1) health system-level facilitators and (2) patient-cognitive factors.Themes and quotations are summarized in Table 2.

Patient interactions with clinicians
Facilitators to surveillance colonoscopy completion included patients receiving reminders and education from clinicians (11 participants [84.6%]) and routine clinician-patient visits (8 participants [61.5%]).Clinicians commented that reminding patients and proactively addressing concerns led to increased colonoscopy completion rates."With insurance changing constantly, like where they accept, or like institutions changing which insurance they cover, if somebody is trying to come back to us for their scope but their insurance has changed and we're no longer covered and then they have to try and establish care, I know that that can be an issue." • Lack of transport/lack of chaperone to procedure 4 (30.8%)"I see a lot sometimes of needing a family member or friend to escort them to the procedure and potentially not having someone, and therefore that being a barrier to having it done."

Organizational factors
The organizational facilitators most cited by clinicians were primary and specialty care integration (6 participants "If they hear it from their doctors or their APP's, I think they know it's important.So we don't just send a letter, in contrast, we say make sure you do this, you know, they hear it directly from us at a visit.And then sometimes when they raise challenges with doing bowel preps, and we can talk them through that and counsel them through, make sure they get the right prep." • Routine interactions with healthcare system 8 (61.5%) "We try to adhere to the guidelines regarding follow up of our patients, and frequency of, and that sort of thing.So that relationship that you have with the patient every few months and that visit is a good opportunity to reinforce the importance of it." Organizational factors • Primary and specialty care integration (organizational) 6 (46.2%) "And then I think having it be an interdisciplinary effort so it's not just the providers but the whole team is sort of aware of the importance, and then it's something that the clinical nurse can follow up with the patient as well, if they're having any delays or any questions, they have that relationship with the nurse too and they can continue the conversation." • EHR tools 4 (30.8%)"We have a health maintenance tab that's in our electronic medical record and it flags if someone is not up to date with their surveillance colonoscopy." • Scheduling accommodations 4 (30.8%)"You know, patients are coming from far away.Maybe they don't want to come over the mountains because the passes are hard to travel, so they're willing to consolidate their visits you know, that are either a little bit earlier or a little bit later." Cognitive factors • Patient motivation to prevent recurrence 7 (53.8%)"I think one is, patient wise, I think there's internal motivation, you know, they're motivated to get their checkups and know that this is part of making sure that they are clear and their cancer is not coming back.And so there's motivation on the patient's part, they have interest in it." • Patient-clinician concordance about colonoscopy importance 3 (23.1%)"The whole group has buy in, the medical oncologist it's part of their pathway.We just have a cohesive care plan that everyone needs to follow, this is the surveillance, we go by NCCN guidelines and everyone's on board to make sure these boxes are checked." Abbreviations: APP, advanced practice provider; NCCN, national comprehensive care network.
T A B L E 2 (Continued)  tools such as reminders also helped facilitate surveillance completion.Clinicians suggested that integrating EHR alerts for surveillance colonoscopies, akin to cancer screening reminders, might enhance completion rates.Scheduling colonoscopies during initial post-operative appointments, patient-owned electronic checklists outlining surveillance needs, and nurse navigation were all identified as potential areas for intervention.

| DISCUSSION
Our study identified several barriers and facilitators to 1-year surveillance colonoscopy completion from the clinician-perspective.All clinicians identified at least one organizational factor as a barrier to surveillance colonoscopy completion, but some organizational factors when present (e.g., primary and specialty care integration), facilitated surveillance colonoscopy completion.Ultimately, clinicians identified several areas for potential intervention to improve 1-year surveillance colonoscopy completion among CRC survivors.To our knowledge, our study is the first to examine clinician perspectives on 1-year surveillance colonoscopy completion.
Our qualitative study provides additional evidence to support some previously reported barriers.For example, one study found that inadequate insurance was associated with lower surveillance colonoscopy completion, which is concordant with our study. 20Given the limited number of studies looking at surveillance colonoscopy barriers in CRC survivors, screening studies could serve as a proxy for identifying potential barriers.Screening studies have identified transportation issues and inflexible work schedules as barriers to colonoscopy completion. 21,22Our study suggests that similar barriers are encountered among CRC survivors who require surveillance colonoscopies.
Clinicians suggested several facilitators to 1-year surveillance colonoscopy completion including routine clinician-patient interactions.Previous quantitative studies have shown that patients who see their PCPs or an oncologist within the first year of a CRC diagnosis are more likely to receive surveillance colonoscopies. 23,24Similarly, physician endorsement is positively associated with obtaining a colonoscopy in the non-CRC population. 25Clinicians offered several potentially modifiable intervention targets to increase 1-year surveillance colonoscopy completion including electronic reminders for clinicians.

| STRENGTHS AND LIMITATIONS
The strengths of this study are its qualitative study design, which allowed for detailed inquiry not otherwise possible through EHR review and its diverse participant population making our results generalizable to clinicians of varying specialties and practice scopes.A limitation of our study was the small clinician sample size from a limited number of regional clinics.

| CONCLUSION
Understanding clinician perspectives is important for the development of effective interventions to improve surveillance colonoscopy completion rates and has the potential to improve outcomes for CRC survivors.
Clinician participant characteristics.Clinician-identified key themes, subthemes, and supporting quotations.Yeah, just anytime we have to coordinate or refer to an outside institution, you know, it, most of the time gets done without a hitch, but sometimes it just requires [more] and it's just more moving pieces.A little bit more on the patient to make sure to receive that call from the other place, and depending on whether the other place calls them in time and communicating what needs to be done with the other institution."Other barriers are health system resources, so you know, we're short staffed, and so we've had to close rooms every once in a while." T A B L E 1 a Four medical oncologists, four colorectal surgeons, and two gastroenterologists.T A B L E 2 "A lot of time you know, when patients have more of a piecemeal care at different place, their local providers might not be that up to date in terms of the recommendation for colorectal cancer surveillance management.And that's really when things get missed."